sign in sign up
<<
Home , Chemosynthesis, RISE project

of pressure and temperature alone limit Rona et al., Eds. (Plenum, New York, 1983), 19. A. Williams, Proc. Biol. Soc. Wash. 93, 443 pp. 735-770. (1980). the activities of deep-sea . 3. Galapagos Biology Expedition Participants, 20. P. Pugh, Philos. Trans. R. Soc. London 301, 165 and the food chains that Oceanus 22, 1 (1979); K. Crane and R. Ballard, (1983); K. Woodwick and T. Sensenbaugh, J. Geophys. Res. 85, 1443 (1980); J. F. Grassle Proc. Biol. Soc. Wash., in press. depend on them have evolved in re- in Hydrothermal Processes at Seafloor Spread- 21. RISE Project Group, Science 207, 1421 (1980); ing Centers, P. A. Rona et al., Eds. (Plenum, F. Gaill et al., C. R. Acad. Sci. 298, 553 (1984); sponse to the rich supply of reduced New York, 1983), pp. 665-676. ibid., p. 331. compounds available for chemosynthe- 4. D. Desbruyeres, P. Crassous, J. Grassle, A. 22. D. Cohen and R. Haedrich, Deep-Sea Res. 30, Khripounoff, D. Reyes, M. Rio, M. Van Praet, 371 (1983). sis. A further constraint is that the ani- C. R. Acad. Sci. 295, 489 (1982). 23. R. Lutz, L. Fritz, D. Rhoads, Eos 64, 1017 mals must continually colonize new 5. R. Ballard, J. Francheteau, T. Juteau, C. Ran- (1983). gan, W. Normark, Earth Planet. Sci. Lett. 55, 1 24. K. Macdonald et al., Earth Planet. Sci. Lett. 48, vents tens and occasionally hundreds of (1981); R. Ballard, T. H. van Andel, R. Hol- 1 (1980). kilometers away. Despite differences in comb, J. Geophys. Res. 87, 1149 (1982); R. 25. K. Turekian, J. K. Cochran, Y. Nozaki, Nature Ballard, R. Hekinian, J. Francheteau, Earth (London) 280, 385 (1979); K. K. Turekian and J. faunal composition and at least partial Planet. Sci. Lett. 69, 176 (1984). K. Cochran, Science 214, 909 (1981); , J. 6. L. Laubier and D. Desbruyeres, La Recherche Bennett, Nature (London) 303, 55 (1983). isolation of vent fields, these communi- 161, 1506 (1984). 26. C. Berg, Bull. Biol. Soc. Wash., in press. ties have had a long evolutionary his- 7. R. Turner and R. Lutz, Oceanus 27, 54 (1984); 27. Observations made by K. Turekian. Florida Escarpment Cruise Participants, ibid., 28. K. Turekian et al., Proc. Natl. Acad. Sci. tory. Fossil vent worm tubes have been p. 32. U.S.A. 72, 2829 (1975). identified in Cretaceous sulfide ores (34), 8. J. Grassle, personal communication. 29. J. F. Grassle and L. Morse-Porteous, unpub- 9. J. McLean, Bull. Biol. Soc. Wash., in press. lished data; H. Sanders and J. Allen, Bull. Mus. and the nearest relative of the archeogas- 10. M. Jones, Oceanus 27, 47 (1984). Comp. Zool. Harv. Univ. 145, 237 (1973). tropod limpets date from the Paleozoic, 11. D. Desbruyeres and L. Laubier, Oceanol. Acta 30. R. D. Turner, Science 180, 1377 (1973). 3, 267 (1980); Proc. Biol. Soc. Wash. 95, 484 31. , personal communication. over 200 million years ago (9). The co- (1982); V. Tunnicliffe, Eos 64, 1017 (1983); per- 32. H. Jannasch and C. Taylor, Annu. Rev. Micro- sonal communication. biol. 38, 487 (1984). occurrence of a clam, a , and a 12. J. F. Grassle et al., Bull. Biol. Soc. Wash., in 33. J. Childress and T. Mickel, Eos 64, 1018 (1983); vestimentiferan worm at widely separat- press. J. Childress and R. Mickel, Mar. Biol. Lett. 3, 13. J. Enright et al., Nature (London) 289, 219 73 (1982); T. Mickel and J. Childress, Biol. Bull. ed sites in the Pacific and Atlantic repre- (1981); P. Lonsdale, Deep-Sea Res. 24, 857 (Woods Hole, Mass.) 162, 70 (1982). sents either an unusual distribution from (1977). 34. R. M. Haymon, R. A. Koski, C. Sinclair, Sci- 14. C. M. Cavanaugh et al., Science 213, 340 (1981); ence 223, 1407 (1984). a single lineage or, even more remark- Nature (London) 302, 58 (1983); H. Felbeck, 35. I thank the crew of DSRV Alvin and S. Brown- ably, cases of parallel evolution. Science 213, 336 (1981); Nature (London) 293, Leger, L. Morse-Porteous, R. Petrecca, and I. 291 (1981). Williams for technical assistance; I thank J. P. 15. P. Comita and R. Gagosian, Nature (London) Grassle, L. Morse-Porteous, and J. M. Peterson References and Notes 307, 450 (1984). for invaluable comments and assistance in the 16. K. L. Smith, 66, 1067 (1985). preparation of the manuscript. The work was 1. J. Brooks et al., Eos 66, 106 (1985); Canadian 17. G. H. Rau, Nature (London) 289, 484 (1981); supported by grants OCE7810458, OCE7810459, American Seamount Expedition, Nature (Lon- and J. I. Hedges, Science 203, 648 OCE8115251, and OCE8311201 from the Na- don) 313, 212 (1985); C. Paull et al., Science 226, (1979); G. H. Rau, ibid. 213, 338 (1981); B. Fry, tional Science Foundation. This is contribution 965 (1984). H. Gest, J. Hayes, Nature (London) 306, 51 No. 5963 of the Woods Hole Oceanographic 2. R. Hessler and W. Smithey, in Hydrothermal (1983). Institution, 71 of the GaI.pagos Rift Biology Processes at Centers, P. A. 18. D. Rhoads et al., J. Mar. Res. 40, 503 (1982). Expedition, and 50 of the Oasis Expedition.

eukaryotic organisms. At the same time, bacteria retain a much wider metabolic diversity than is found in plants and . Because of the resulting bio- chemical versatility of natural microbial Geomicrobiology of Deep-Sea populations and the smallness, general resistance, and dispersibility of bacterial Hydrothermal Vents cells, these organisms are able to exist in more extreme environments than the higher organisms. Therefore, the occur- Holger W. Jannasch and Michael J. Mottl rence of certain microorganisms at deep- sea vents was predictable; however, their ability to make it possible for higher forms of life to thrive with an unusual Deep-sea hydrothermal vents were tures of 2700 to 380°C and flow rates of 1 efficiency on inorganic sources of energy discovered in the 1970's after an exten- to 2 m sec'1. Hot vent fields commonly in the absence of light was entirely unex- sive search along the GalApagos Rift (1, include warm- and intermediate-tem- pected. 2), a part of the globe-encircling system perature vents (0300TC) ("white smok- of sea-floor spreading axes. During the ers") as well as high-temperature vents past 7 years, more (3500 ± 20C) ("black smokers"). A high- Chemosynthesis fields have been located along the East ly efficient microbial utilization of geo- Pacific Rise. They fall into two main thermal energy is apparent at these The most significant microbial process groups: (i) warm vent fields with maxi- sites-rich populations were taking place at the deep-sea vents is mum exit temperatures of 50 to 23°C and found to be clustered around these vents "bacterial chemosynthesis." The term flow rates of0.5 to 2 cm sec'1 and (ii) hot in the virtual absence of a photosynthetic was coined by Pfeffer in 1897 (6) in vent fields with maximum exit tempera- food source (3-5). obvious contrast to the then well-known Microorganisms, mainly bacteria, are . Both processes involve efficient geochemical agents. As pro- the of carbon com- Holger W. Jannasch is a senior scientist in the biosynthesis organic Biology Department and Michael J. Mottl, is an karyotic organisms, they lack a mem- pounds from C02, with the sour'ce of associate scientist in the Chemistry Department at Woods Hole Oceanographic Institution, Woods brane-bound nucleus and thereby the energy being either chemical oxidations Hole, Massachusetts 02543. complex genetic apparatus of the higher, or light, respectively. More specifically, i2 AUGUST 1985 717 Table 1. Electron sources and types of chemolithotrophic bacteria potentially occurring at the crust is responsible for the wide hydrothermal vents. range of exit temperatures (2, 10). Thus, chemical species that are nonreactive Electron donor Electron Organisms during mixing define mixing lines as a function of temperature for the warm S2-, SO, S2032 02 -oxidizing bacteria S2-, 2 N03- Denitrifying and sulfur-oxidizing bacteria vent waters. These lines pass through SO, S203 ambient seawater and extrapolate to a H2 02 -oxidizing bacteria at 350°C similar to that actu- H2 NO3- Denitrifying hydrogen bacteria composition H2 S, S042- Sulfur- and sulfate-reducing bacteria ally measured in the hot vent waters. H2 CO2 Methanogenic and Most of the chemical species thought acetogenic bacteria in NH4+, N02 02 Nitrifying bacteria to participate microbiological reac- Fe2+, (Mn2+) 02 Iron- and manganese-oxidizing bacteria tions do not exhibit such linear mixing CH4, CO 02 Methylotrophic and carbon monoxide- behavior. These species may therefore oxidizing bacteria originate either at depth in the high- temperature end-member solution that has been produced by reaction of heated seawater with crustal rocks (11), or they chemoautotrophy refers to the assimila- bolic mechanism required for generating may originate in the shallow subsea-floor tion of CO2 and is coupled in some the necessary negative potential. region, either directly from bottom sea- bacteria to chemolithotrophy, the ability Some organisms have the ability to use water or as a result of various inorganic to use certain reduced inorganic com- organic compounds simultaneously as and organic reactions that occur on mix- pounds as energy sources. electron sources (mixotrophy). Since in ing (Fig. 1). In the present-day terminology, the autotrophy carbon (CO2) must be re- The concentrations of relevant species relation between photosynthetic and duced from a higher oxidative state than from the best-studied hot vent fields chemosynthetic is illustrated organic carbon, more energy is required (those on the near in the following schematic equations, than in heterotrophy. Therefore, obligate 21°N) and warm vent fields (those on the where the reduced carbon is represented chemoautotrophic bacteria generally Galapagos Rift near 86°W) are shown in as a , [CH2O]: grow more slowly than or Table 2. Also shown are the results of require larger amounts of substrate in two model calculations, the first for a 2C02 + H2S + 2H2 h.- terms of energy supply. conservative mixture of the hot vent 2 [CH20] + H254 (1) During recent years a number of new waters with bottom water and the (nonoxygenic photoautolithotrophy, types of anaerobic chemoautotrophic second for the same mixture after some purple and green bacteria) bacteria have been isolated and de- simplified inorganic reactions have oc- scribed. Among them are , curred. h' CO2 + H20 1 [CH2O] + 02 (2) acetogens, and sulfate-reducing bacteria The prominence of H2S is obvious (oxygenic photoautolithotrophy, (7). In addition, it has been shown that from Table 2. There are two possible green plants) certain extremely thermophilic methano- sources for H2S in the hot vent waters: it gens are able to respire elemental sulfur may be leached from crustal , or it CO2 + H2S + 02 + H20- (8, 9). All these metabolic types are may be produced by reduction of S042- [CH2O] + H2SO4 (3) potential catalysts of geochemical trans- from seawater coupled with oxidation of (aerobic chemoautolithotrophy, bacteria) formations at deep-sea vents. Fe2+ from to Fe3+. Both mecha- All the inorganic energy sources listed nisms are important in laboratory experi- 2CO2 + 6H2 in Table 1 have been found in hydrother- ments at 300°C and above, but they [CH2O] + CH4 + 3H20 (4) mal fluids or in waters surrounding the occur only sluggishly or not at all at (anaerobic chemoautolithotrophy, bacteria) vents except thiosulfate, the occurrence lower temperatures (12). It is likely that of which has not been specifically stud- both mechanisms are important in the From an evolutionary point of view, ied. Before discussing those types of natural system as well. The concentra- reactions 1 and 2 above are bridged by bacteria that have been isolated and tion of sulfur in typical mid-ocean ridge the blue-green or cyanobacteria. In aero- those microbial processes that have been basalt (-25 mmol/kg as S2-) is similar to bic chemosynthesis, the possible elec- shown to occur, we will outline the hy- that in seawater (-28 mmol/kg as tron donors used by a large variety of drothermal origin and the documented S042-), and seawater circulating through bacteria are listed in Table 1. Some of occurrence of the critical inorganic spe- the hydrothermal system of a mid-ocean them are the same as those used in cies. ridge apparently reacts with an amount anaerobic chemosynthesis where free offresh rock about equal to its own mass is replaced by NO3-, elemental (10, 13, 14). Although the hot vent wa- sulfur, s042-, or CO2 as electron accep- Sources of H2S and Structure of the ters are essentially free of S042-, circu- tors. The inorganic sources of energy are Mixing Region lating seawater can be expected to lose used for the production of ATP (adeno- some or all of its load of s042- as sine 5'-triphosphate), akin to the use of The chemistry of the vent waters indi- anhydrite (CaSO4), which precipitates light in phototrophy. cates that both warm and hot vent fields on heating to temperatures as low as Differences in the average growth are fed at depth by a high-temperature 130°C (15). Thus, little seawater s042- rates of chemolithotrophic bacteria un- end-member solution at about 350°C and may be delivered to the deeper, hotter der comparable conditions are deter- that the mixing of this solution with parts of the system where it could be mined by the amount of energy required largely unreacted and unheated ocean reduced to S2-. Sulfur isotopic analyses for "reverse electron transfer," a meta- bottom water in the shallow regions of of H2S from the hot vent waters and of 718 SCIENCE, VOL. 229 sulfide minerals from the precipitated lenium go to zero; at lower tempera- lower than the sulfide-related elements vent chimneys indicate that H2S is de- tures, these species are apparently un- and slightly above the highest tempera- nved mainly from the basalts, but that reactive and thus define mixing lines ture sampled; thus the reservoir is free of the seawater source also is important with ambient seawater. N03- and is anoxic because of the reac- (16). The NO3- concentration extrapolates tion of these species from seawater with The conservatively calculated H2S to zero at a temperature just slightly H2S and other reduced species from the concentration in Table 2 for a 12.6°C mixture of hot vent water with seawater is in the same range as those in the warm vent waters at the same temperature. Summary. During the cycling of seawater through the earth's crust along the mid- H2S undoubtedly is not conservative ocean ridge system, geothermal energy is transferred into chemical energy in the during subsurface mixing, however, as form of reduced inorganic compounds. These compounds are derived from the Fe2+, 02, and N03- are all heavily de- reaction of seawater with crustal rocks at high temperatures and are emitted from pleted in the warm vent waters, presum- warm (<25°C) and hot (-350°C) submarine vents at depths of 2000 to 3000 meters. ably as a result of reaction with H2S. Chemolithotrophic bacteria use these reduced chemical species as sources of energy Examination of the relation between for the reduction of (assimilation) to organic carbon. These bacteria vent temperature and the concentrations form the base of the , which permits copious populations of certain of species that react on mixing in the specifically adapted invertebrates to grow in the immediate vicinity of the vents. Such shallow subsea-floor provides insight highly prolific, although narrowly localized, deep-sea communities are thus main- into the structure of the shallow crustal tained primarily by terrestrial rather than by solar energy. Reduced sulfur compounds mixing region and the chemical process- appear to represent the major electron donors for aerobic , but es that occur there. This mixing region, -, hydrogen-, iron-, and manganese-oxidizing bacteria have also been found. with its large area of basalt surfaces, Methanogenic, sulfur-respiring, and extremely thermophilic isolates carry out anaero- which serve as substrate, and its dual bic chemosynthesis. Bacteria grow most abundantly in the shallow crust where source of electron donors from the hot upwelling hot, reducing hydrothermal fluid mixes with downwelling cold, oxygenated water end-member and electron accep- seawater. The predominant production of , however, is the result of symbiotic tors from seawater, is a major site of associations between chemolithotrophic bacteria and certain invertebrates, which microbial production. have also been found as fossils in Cretaceous sulfide ores of ophiolite deposits. The generalized relation is shown in Fig. 2. For a given vent field, 02 and NO3- decrease linearly from their values in ocean bottom water to zero at charac- teristic temperatures <20'C that vary from one vent field to another (Table 3). H2S decreases linearly with decreasing temperature as 02 and N03- increase, generally going to zero at the bottom- water temperature of 2°C. An inflection typically occurs in the H2S-temperature relation where 02 goes to zero, with the slope of the H2S temperature curve be- coming steeper at higher temperatures. Other species whose concentrations de- crease from their seawater values and extrapolate to zero at temperatures -<20 to 30°C in the warm vent waters are chromium, uranium, nickel, , cad- mium, and selenium (10). Thus distinct zones exist in the shal- low subsea-floor mixing region that are characterized by particular redox condi- tions; in some cases the boundaries be- tween these zones are abrupt and iso- thermal (Fig. 2). Edmond et al. (10) have inferred that a shallow subsurface reser- voir at 100 to 32°C is located beneath the warm vent fields and is being tapped by the vents. The temperature range of this reservoir is defined by the lowest tem- peratures at which specific chemical pro- cesses occur. The inferred processes are Fig. 1. Schematic diagram showing inorganic chemical processes occurring at warm- and hot- listed in Table 3. The minimum tempera- water vent sites. Deeply circulating seawater is heated to 3500 to 400°C and reacts with crustal tures at which sulfide deposition occurs basalts, leaching various species into solution. The hot water rises, reaching the sea floor directly in some places and mixing first with cold, downwelling seawater in others. On mixing, in the subsea-floor reservoir are those at iron-copper- sulfide minerals and anhydrite precipitate. Modified from Jannasch and Taylor which nickel, copper, cadmium, and se- (54). 23 AUGUST 1985 719 hot-water end-member. The 02 concen- Sources of Other Chemical Species tration goes to zero at a temperature 10 to Used in Chemosynthesis 11°C lower than N03 , depending on the vent field (Table 3). In addition to H2S, the subsea-floor These observations are best explained reservoir contains H2 (17), although in in terms of two distinct zones that are much lower concentrations than would shallower than the reservoir itself, in be expected from the high values in the which the residence time of the mixed hot-water end-member (Table 2). When waters is short relative to the rate of seawater was reacted with basalts in reduction of N03- or NO2- and 02, laboratory experiments (18), the result- respectively. The warmer zone 0 4 8 12 16 was probably Temperature (OC) ant concentration of H2 lower than consists of the channels that connect the Fig. 2. Relation between temperature and the that in the natural 350°C solutions. It sea 02 reservoir to the floor, in which iS concentrations of 02, NO3-, and H2S defined apparently was controlled by the redox reduced completely but N03- is largely by samples from individual vents in a single state, which was near the magnetite- nonreactive. Both N03- and H2S coex- warm vent field. The specific values shown hematite boundary at 3500 to 375°C. The ist in this zone (Fig. 2), which was fre- vary from field to field, but the topology is typical and has been generalized from the H2-02 redox couple approached equilib- quently sampled directly. The cooler seven fields on the Galapagos Rift listed in rium faster than any other redox couple. zone probably consists of the throats of Table 2. Labels refer to inferred zones within Isotopic data on H2 from the hot vent the vents themselves, in which the resi- the subsea-ftoor mixing region. waters also suggest a close approach to dence time is so short that all species mix equilibrium for H2-H20 (12). Inorganic conservatively; H2S, 02, and NO03 co- reaction of H2 with 02 from seawater to exist in this zone. floor reservoir. The uniformity of the relatively low temperatures during mix- Samples from several vents within a characteristic temperatures for different ing could easily account for the relatively single vent field define single mixing vents within a single vent field reinforces low H2 concentrations in the warm vent lines for reactive species. This implies the notion of a subsurface reservoir cre- waters, which may then have been af- that the temperatures that bound the ated by permeability variations in the fected by bacterial reactions. various zones are uniform across the shallow subsea-floor. In contrast to H2, CH4 and CO are area of an individual vent field. Variation Because the inferred reservoir is present at much higher concentrations in in these characteristic temperatures from anoxic, like the water in the surficial the warm vent waters than would be one field to another (Table 3) may reflect upflow channels, aerobic chemosynthet- expected from the concentrations in the to some extent the variations in composi- ic microorganisms probably thrive main- hot vent water (Table 2). CH4 in the hot tion of the hot-water end-member feed- ly at the margins of these zones, where vents is almost certainly abiogenic, on ing the various fields. Probably, howev- downwelling oxygenated seawater mixes the basis of its similar concentration in er, this variation is mainly a function of with the major bodies of already mixed fresh basalts and its relatively heavy the shallow crustal channel geometry and reacted solutions. Electron-donor isotopic composition (19), although in- and the distribution of permeability and species from the reservoir would be terpretation of the isotopic data has been recharge rates of seawater to the subsea- available at these sites. questioned (17). No isotopic data are

Table 2. Comparison of the compositions of actual warm vent water at several vent fields with those calculated as mixtures of hot (350°C) vent water with seawater (concentrations in micromoles per kilogram of solution). Vent fields: Ocean Bottom Seismograph (OBS), Southwest (SW), and Hanging Gardens (HG), all on the East Pacific Rise near 21°N; Clambake (CB), Garden ofEden (GE), Dandelions (DL), and Oyster Bed (OB) sampled in 1977, plus Mussel Bed (MB), East of Eden (EE), and Rose Garden (RG) sampled in 1979 on the Galipagos Rift near 86°W. End-members Mixtures at 12.60C

350°C waters Compo- conservative position: reacted* 12.6°C = 800 M Si)

Refer- OBS SW HG OBS SW HG OBS SW HG CB GE DL OB MB EE RG ence Vent waters IH2S 7300 7450 8370 219 224 251 105 127 102 20 120 260 50 500 180 (10, 11, 17) H2 1700 380 51 11 0 0 0 0.12 0.03 (17, 19) CH4 45 53 1.4 1.6 3.1 8.8 2.4 (17, 19) CO 0.31 0.67 0.0009 0.02 0.06 0.39 0.06 (17) NH3 <10 <10 <10 <0.3 <0.3 <0.3 4 4 4 2.8 0.0 2.8 0.0 (11, 17) NO2- <0.1 <0.003 2 2 2 1.3 8.2 (11, 17) N20 <0.02 0.06 <0.0006 0.0002 0.13 0.00 0.03 (17) Fe2+ 1664 750 2429 50 23 73 0 0 0 30 0.5 -3 <1 (10, 11) Mn2+ 960 699 878 29 21 26 42 11 16 15 (10, 11) £CO2 5720 2400 2510 2580 (13) Ambient seawater 02 107 104 0 0 0 0 0 0 0 0 0 0 (10, 17) N03 39 38 0 0 0 0 1.0 0 0 0 11.5 (10, 17) XCO2 2300 (11) Temperaturet (°C) 2.2 9.3 12.1 6.6 9.1 10.0 5.6 16.4 (10, 17) *The reaction sequence used is: 2H2 + 02- 2H20; Fe2+ + -* FeS + 2H+; 49H S + 76NO3- + 8H20-. 32N2 + 8NH4+ + 4NO2- + 49S42- + 18H+ + 32H20; H2S + 202 - So042- + 2H+. tTemperatures are for ambientH;S seawater and for the highest temperature sample used in this data compilation. 720 SCIENCE, VOL. 229 Table 3. Temperatures at which the concentrations of various species in seawater decrease to zero in warm vent fields on the Galapagos Rift near 86°W (10, 17). The temperature at which N03 goes to zero is considered to be the best estimate for the isotherm that bounds the shallow subsea- floor reservoir underlying the various vent fields. See Table 2 for the names of the fields. Temper- Vent field Species Inferred locality and process ature (OC) RG GE MB CB DL OB EE Cr Reservoir: CrlV042-__ Cr2111O3 -32 U Reservoir: UVIO2(CO3)34-_+ UIVO2 -24 Se Reservoir: substitution in sulfide -20 minerals Ni, Cu, Cd Reservoir: precipitation as or in sulfide 12.5-13.5 14.4-24.2 9.9-12.2 minerals N03- Reservoir: reduction by H2S 18.0 12.6 12.4 10.7 9.9 8.6 02 Reservoir and upflow channels: 6.9 9.5 9.2 9.3 6.5 6.3 3.7 reduction by H2S Maximum temperature sampled 16.4 12.7 10.0 9.3 6.6 9.9 5.6 available for CH4 or CO from the warm N2. NH4' and NO2- behave linearly prevented, we were unable to find signif- vents, but the anomalously high concen- versus temperature over the entire inter- icant numbers of microscopically visible trations of these two species could well val sampled for some warm vent fields bacteria in hot (3380 to 350°C) vent wa- indicate a primarily biological origin, (for example, Clambake); for others, ter. In contrast, 4.7 x 105 cells were probably in the anoxic subsea-floor res- however (NO2- in Oyster Beds), they counted in vent water at 304°C (21) when ervoir. As with N03-, CH4 behaves lin- display inflection points indicating their the temperature was determined from early with temperature over the entire consumption in the upflow channels. magnesium concentrations (22). This interval sampled (17), indicating that, Thiosulfate has not been sought, but finding indicated an unspecified amount unlike H2S and 02, it is conserved in the elemental sulfur has been detected in of seawater intrusion prior to or during inferred channels to the sea-floor. In at warm vent effluent as well as in the sampling. least one warm vent field (Rose Garden), chimneys of black smokers and white Since aerobic chemosynthesis results CO apparently is produced in the upflow smokers. The slopes of plots of H2S in higher than anaerobic channels, as indicated by its inflection versus temperature for those warm vent chemosynthesis, the availability of the point and slope when plotted against samples that are free of 02 suggest that electron donor and oxygen under favor- temperature. sulfur species with intermediate oxida- able growth conditions will be decisive. The reservoir also contains Fe2' and tion states are being formed on mixing as From this point of view, bacterial pro- Mn21 in substantial concentrations, de- well as so42-, although so42- is usually ductivity should be highest in the vicinity rived by leaching from basalt at high dominant. Seawater also contributes of warm vents where the slow emission temperature. Mn2+ plots linearly against S042- directly to the subsea-floor reser- of sources of reduced chemical energy temperature over the entire interval sam- voir. into oxygenated seawater forms slowly pled for the warm vents (10), and these Among the electron acceptors, CO2 is moving plumes. In contrast, the forceful lines extrapolate to concentrations simi- paramount. This species is highly en- emission of hydrothermal fluid from the lar to those in the 350°C end-member riched in the hot vent water by the hot vents results in a quick dispersal and (Table 2). Thus, Mn2+ is largely nonreac- leaching of CO2 from basalt (19, 20). Its fast dilution of energy sources in the tive in the shallow subsea-floor. Fe2+, by concentration in the warm vent waters is water column, eventually leading to contrast, is nonlinear over the sampled about what it should be if the behavior of chemical oxidations. The observation of interval in the same sense as H2S (Fig. CO2 on mixing is conservative (Table 2). maximum populations of animals in the 2); thus it is being removed from solution immediate vicinity of warm vent plumes in the upflow channels as well as in the and heavy bacterial mats near warm reservoir, probably by a combination of Microbial Populations of leakages at the base of hot vent chim- sulfide and oxide deposition. It is uncer- Emitted Vent Waters neys supports these assumptions. tain to what extent Fe2+ is utilized in Biomass measurements can also be microbiological reactions, as it readily Without considering their specific cat- based on determinations of adenosine participates in inorganic reactions under alytic function, one can assess abun- triphosphate (ATP) or total adenylates these conditions. dance of natural bacterial populations by (22). Data of Karl et al. (5) demonstrate Other electron donors present in the determining cell concentrations or by that the microbial biomass of warm vent subsea-floor reservoir do not originate measuring growth rates using unspecific plumes, determined as ATP, was two to mainly from the hot-water end-member. tracers. The milky-bluish waters (Fig. three times that of the photosynthetic- NH4+ and NO2- were at or below detec- 3A) flowing from some of the warm heterotrophic microbial populations of tion limits in the 350°C solutions but vents (60 to 23°C, 1 to 2 cm sec- 1) surface waters at the same site (Galapa- were readily measurable in the warm contain between 105 and 109 cells per gos Rift). The ratio of guanosine 5'- vent waters (Table 2). They almost cer- milliliter (2, 4, 5). Independent of the triphosphate to ATP, also measured in tainly derive from reduction of seawater temperatures measured, the large range this study (5), has been interpreted as an N03- introduced into the reservoir, by of numbers is due to the dilution of vent indicator of growth rates. It correlated reaction mainly with H2S. Also present water at the point of sampling. Visible well with the data derived from biomass at very low concentrations is N20 (17). bacterial aggregates add to this heteroge- determinations (5). These species together account for less neity and may represent dislodged pieces The most recent developments in the than 20 percent of the introduced NO37; of microbial mats (4, 5). When contami- measurement of growth rates of natural most ofthe rest is presumably reduced to nation by ambient water was strictly microbial populations are based on the 23 AUGUST 1985 721 use of tritiated nucleotides (adenine or ception to this rule: the common occur- the aid of the research submersible Al- thymidine) for incorporation into RNA rence of the genus Thiobacillus appears vin, arrays of six 200-ml syringes were and DNA (23). It is assumed that the to be replaced by a prevalence of the filled in situ from a joint inlet (27). They assimilation of these marker substrates genus Thiomicrospira (25). facilitated replica and control samplings does not affect growth by stimulating Pure-culture isolations resulted in a and were used for in situ incubation ATP production. In a recent study with wide range of metabolic types of sulfur experiments (Fig. 4). At the base of the samples collected from a hot smoker bacteria including acidophilic obligate 21°N black smoker, the in situ rate of orifice, higher adenine incorporation chemoautotrophs, (which CO2 incorporation by natural microbial rates were found at 90°C than at 210 and simultaneously assimilate inorganic and populations in warm water leakages was 50°C (24). organic carbon), and facultative chemo- approximately 10-6 pLM ml-' day-' (27). In addition to their occurrence in (25). Since the presence of When parallel samples were incubated in warm vent water plumes (Fig. 3A), large organic carbon can be expected to be the ship's laboratory (atmospheric pres- microbial populations are also found (i) widespread within the vent communi- sure) at 3°C, the rate was virtually the as mats covering almost indiscriminately ties, the facultative chemoautotrophs same (indicating a minimal effect of hy- all surfaces exposed to warm vent may well represent the predominant type drostatic pressure). This result was cor- plumes (Fig. 3, B and C) and (ii) in of sulfur bacteria. The demonstrated ex- roborated by data on the metabolic rates symbiotic tissues within certain vent in- cretion of organic carbon by obligate of a pure culture isolate (Thiomicrospira, vertebrates (see below). Quantitative chemoautotrophs indicates the possible strain L-12) as affected by pressure (24). data on microbial activities at these two occurrence of these bacteria even in the In a second shipboard incubation at sites have not yet been obtained. subsurface vent systems (25). The pref- 23°C, the in situ temperature of the erence for a neutral pH range favors warm-water leakages, the rate of CO2 the facultative (polythionate-producing) incorporation increased one and a half Sulfur-Oxidizing Bacteria and chemoautotrophs in the well-buffered orders of magnitude (27). This behavior Rates of Chemosynthesis seawater environment (26). This bio- indicates the "mesophilic" growth char- chemical versatility of sulfur bacteria, acteristic of the total natural population. The predominant chemosynthetically together with the relatively high concen- A similar response was found in pure usable chemical energy at the vents ap- trations of reduced sulfur compounds, cultures. An addition of 1mM thiosulfate pears in the form of sulfur compounds. appears to be the key to their predom- as an accessory energy source in all This predominance is reflected in the inance at the vents and to their role as three experiments resulted in substantial ease and success with which sulfur-oxi- primary chemosynthetic producers com- rate increases. This immediate use of dizing bacteria can be isolated (25). In pared to the other types of chemolitho- reduced sulfur confirmed the predom- general, the types of sulfur bacteria autotrophic bacteria. inance of sulfur-oxidizing bacteria in the found at the deep-sea vents do not differ As in the measurement of photosyn- natural population (27). greatly from those isolated from other thesis, 14CO2 was used as a substrate to Different types of dense bacterial mats H2S-rich environments. There is one ex- determine rates of chemosynthesis. With have been observed at various vents

Fig. 3 (left). (A) Filtrate (bacterial cells) ofturbid water emitted from a warm vent (Mussel Bed, Galpagos Rift vent site, 21°C) on a Nuclepore filter (pore size, 0.2 ,um; scale bar, 1 ,um). (B) Scanning electron micrograph of a grown within a warm vent plume: a, Beggiatoa; b, Thiothrix-like filaments; c, stalks of prosthe- cate cells (Hyphomonas) (scale bar, 5 ,uam). (C) Transmission electron micrograph of the outer surface of a hot vent chimney: a, Methyloloc- cus-type cells with an internal membrane structure; b, mostly thick- walled Thiothrix-like filaments embedded in ferromanganese deposits (scale bar, I R,m). Fig. 4 (right). At left, syringe array for the in situ incubation of six parallel vent water samples to measure rates of 14CO2 assimilation; at right, , most of the tubes with gills extended; tube length, 0.5 to 1.0 m. Location: warm vent at the base of a black smoker at 21°N, 109°W; depth, 2610 m; Alvin dive 1223. [Photo by D. M. Karl] 722 SCIENCE, VOL. 229 (28). The genera Thiothrix and Beggiatoa morphological characteristics were ob- An extremely thermophilic methano- appear to be predominant according to served in transmission electron micro- gen of the genus Methanococcus was morphological criteria. During prepara- graphs from bacterial mats (Fig. 3C) (28). isolated from the base of the 21°N black tions for the isolation ofthese organisms, Up to 20 percent of the cells surveyed in smoker (Fig. 4) (38). This the capacities of marine Beggiatoa for sections of mats collected from various showed an optimal growth rate of 0.036 the fixation of N2 and for facultative parts of the vents showed the paired hour' (a doubling time of 28 minutes) at chemolithoautotrophy have been dem- vesicular membranes that distinguish 86°C. These results demonstrate the ex- onstrated (29). Whitish microbial mats methanotrophic cells from similar struc- istence of a potential biological CH4 pro- and streamers were commonly observed tures found in ammonium oxidizers. duction at the vents. The absence of at the base of hot vents. They represent Both CH4- and methylamine-oxidizing isotopic evidence in support of this sites of substantial chemosynthetic pro- bacteria were successfully isolated from observation is not necessarily conclusive duction and active grazing by a variety of microbial mats, filtered vent water, clam because of microbial patchiness. invertebrates. gill tissue, and Riftia (see Although denitrifying H2 oxidizers Thick mats of Beggiatoa-like fila- below), and the pure cultures obtained may exist in vent systems wherever the ments, partly floating above the bottom, were preliminarily grouped as type I NO3-containing bottom seawater mixes were observed in situ at exploratory methanotrophs (33). with rising hydrothermal fluid, the dives at the Guaymas Basin vent site So42-_ and sulfur-reducing equivalents (2000 m deep) in the Gulf of California are geochemically more significant. Both (30). Collected and fixed specimens Hydrogen as a Microbial metabolic types of bacteria do exist but showed a filament width of up to 100 ,um. Source of Energy have not yet been isolated from vent At this site, hot vents are overlayed by waters. The respiration of elemental sul- about 200 m of sediment. A substantial Many different types of microorga- fur has recently been demonstrated to be input of photosynthetically produced or- nisms oxidize H2, but only a few are able a common property of extremely ther- ganic matter from the water column to to use the energy gained for the fixation mophilic methanogens and other archae- the sediments further distinguishes this of CO2 and can be described as chemo- bacteria (8, 9). Above temperatures of site from all others studied so far. High (Table 1). Within this -80°C, this microbial sulfur respiration concentrations of NH3 (-4 mM) have group the term "H2 bacteria" is used occurs in addition to an abiological re- also been reported (31), suggesting che- only for aerobic organisms. Formerly duction. mosynthesis by nitrification. A major grouped in the genus Hydrogenomonas, geochemical-biological study of this site the aerobic H2-oxidizing bacteria are is planned for mid-1985. spread over many known genera (35). All Microbial Iron and Manganese Oxidation of them are facultative autotrophs. As such, they possess ecological advantages Deposits of iron and manganese ox- Microbial CH4 Oxidation similar to those for the facultatively ides cover most surfaces exposed inter- autotrophic sulfur-oxidizing bacteria. mittently to plumes of hydrothermal and Next to reduced sulfur, CH4 may be a They combine the properties of hetero- bottom seawater or to mixes of the two. substantial source of energy for chemo- trophic growth with the use of the Calvin The color of these encrustations ranges synthesis at those vents where cycle enzymes. The net equation for from almost black to light brown. Scan- it has been reported to be present in autotrophic growth is 6H2 + 202 + CO2 ning electron microscopy reveals dense considerable quantities. Although quan- [CH20] + 5H20. microbial mats. A large variety of micro- titatively less abundant than H2 in the Little is known about the ecology of bial forms are deeply embedded in the high-temperature vents, CH4 is more aerobic hydrogen bacteria except that metal oxide deposits (Fig. 3, B and C). abundant in the warm vents (Table 2). their occurrence in nature is as wide- Not enough data exist to permit esti- Evidence for its microbial oxidation is, spread as that of biological H2-producing mates of the rate of mat formation. How- at this time, stronger than that for H2 processes. As in the case of sulfide oxi- ever, when various types of materials oxidation. dizers, the chemosynthetic use of geo- (glass, plexiglass, steel, membrane fil- Methanotrophic bacteria are included thermally produced H2 at the vents rep- ters, and clam shells) enclosed in a pro- in the disparate group of the methylo- resents a of organic tective rack were placed into the opening trophic microorganisms, which comprise carbon. No specific study of aerobic of an active warm (21°C) vent for -10 all those metabolic types that metabolize hydrogen bacteria at the vents has yet months, all surfaces were evenly black- Cl compounds (32). CH4 may serve as been undertaken. An organism with a ened (28, 30). the source of both energy and carbon strong growth stimulation by H2 was Nondispersive x-ray spectroscopy (2CH4 + 202 -* 2[CH2OJ + 2H20), but isolated incidentally from a Riftia tro- showed a decrease of the Fe2+/Mn2+ CO2 may be incorporated as well. All phosome sample (36). ratio in these layers with increasing dis- methanotrophs are strictly aerobic, of- Anaerobic hydrogen-oxidizing bacte- tance from vent openings (28), an obser- ten microaerophilic (33), Gram-negative ria are known as methanogens and aceto- vation attributable to the different sol- rods, cocci, or vibrios and are character- gens because of their products (Table 1). ubility products of the two metals. X-ray ized by typical intracellular membrane They are commonly found at anoxic diffraction determinations of the depos- structures. Methane-utilizing bacteria niches where CO2 and H2 are present as its resulted in a correlation with the miner- may also co-oxidize the CO that may the result of . In hydrother- al todorokite, (Mn,Fe,Mg,Ca,K,Na2) - occur in vent water (17), without gaining mal fluid both compounds are produced (Mn5O12) * 3H2O, which, in its fine- energy in the form ofcell carbon through geothermally. The production of CH4, grained and poorly crystalline state, is enzymes that normally catalyze other H2, and CO was observed experimental- characteristic of marine ferromanganese processes (34). ly at about 100°C in certain media inocu- deposits. Microbial CH4 oxidation at the vents lated with samples of black smoker wa- The role of bacteria in the oxidative was first suggested when the typical ter (37). deposition of iron is difficult to prove in 23 AUGUST 1985 723 neutral or alkaline waters where Fe2+ organisms by their specific ribosomal collected samples. The temperatures of undergoes rapid spontaneous oxidation RNA nucleotide sequences (41). these nongeothermal seepages are near in contact with dissolved oxygen. Het- A heterotrophic bacterium that grows ambient, that is, about 0.15°C above erotrophically grown bacteria have been on a complex organic medium (peptone ambient when measured at a depth of 10 shown to accumulate Fe3+ deposits, but and yeast extract) in a temperature range cm in the sediment. no physiological significance of this from 550 to 98°C with an optimum at From the distribution pattern of inver- process has ever been demonstrated in -88°C has recently been isolated from a tebrates at the tectonic vent sites, it the marine environment. shallow marine hot spring as well as from appears that the spotty occurrence of Although iron lithotrophy has been deep-sea vents (40). It has the facultative elevated temperature is of secondary im- demonstrated for acid freshwaters and respiration of elemental sulfur and some portance for the of these pop- soils, true manganese lithotrophy has not other characteristics in common with the ulations. The overriding factors seem to been proven (39). The oxidation of Mn2+ methanogenic archaebacteria (19). The be the availability of inorganic chemical in seawater (pH -8.1) is more likely than methanogenic vent isolate discussed species and the efficiency of their use in the biological oxidation of Fe2+. Two above (38) differs from all other archae- chemosynthesis. bacterial isolates from the Galapagos bacteria in having a unique macrocyclic Rift vent region oxidized Mn2+ either in glycerol diether instead of a tetraether as growing cultures or in cell extracts (39). the polar membrane (42), which is Symbiotic Chemosynthesis The oxidation was heat-labile and inhib- suspected of affecting the membrane flu- ited by azide (NaN3), potassium cyanide idity at high temperatures. One major evolutionary development (KCN), and antimycin A. The "oxi- Bacterial growth at temperatures up to is responsible for the unusual amounts of dase" was inducible by reduced manga- 250°C by a natural population collected biomass found at the deep-sea vents: a nese and was not constitutive as in iso- from a hot vent has also been reported, new type of between chemo- lates obtained from manganese nodules. but the experimental proof of this study synthetic bacteria and certain marine in- Since ATP synthesis was coupled with is still being contested (21). Other studies vertebrates. Symbiosis is not commonly Mn2+ oxidation it appears that Mn2+- with natural populations collected from a topic ofgeomicrobiology, but this new- oxidizing bacteria do contribute to the the immediate vicinity of hot vents re- ly discovered highly efficient transforma- chemosynthetic production at deep-sea sulted in the microbial production of tion of geothermal or geochemical ener- hydrothermal vents. gases at 100°C (37) and in the incorpo- gy for the production of organic carbon ration of adenine into RNA and DNA at poses a new situation. rates that were higher at 90°C than at 21° The predominant part of the biomass The Role of Elevated Temperatures and 50°C (24). It has also been speculat- observed at the warm deep-sea vents is ed that the particular conditions of deep- generated by the symbiotic association The transfer of thermal to chemical sea hydrothermal vents might lead to a of prokaryotic cells in the clam Calpyto- energy takes place at temperatures synthesis of organic compounds and ulti- gena magnifica and the pogonophoran above 350TC (Fig. 1). Thermophilic C02-, mately to the origin of life (43). tube worm Riftia pachyptila (46) (Fig. 4). so42--, and So-reducing bacteria that Thorough analysis of particulate or- The microbial symbionts have not yet use H2 as the source of electrons (Table ganic carbon has only been done at con- been isolated, but their prokaryotic na- 1) are the best candidates for possible siderable distances from warm vent ture, DNA base ratio, genome size, and microbial activities in hot zones where emissions (44). The results demonstrated enzymatic activities identify them as bottom seawater mixes below the sur- a rather quick passage and complete bacteria (36, 47). They are found within face with rising hydrothermal fluid. Mi- transformation of microbially produced the gill cells of C. magnifica and, as a crobial growth has been measured so far organic compounds into those character- separate "trophosome" tissue, within at temperatures up to H10°C in cultures istic of certain grazers (zooplankton). the body cavity of R. pachyptila. The of extremely thermophilic bacteria iso- Concern about bacterial growth at hot trophosome may amount to 60 percent of lated from shallow and deep marine hot vents is not so much a question ofwheth- the worm's wet weight. vents (40). er there is a substantial addition to pri- The animal's dependence on the mi- The free 02 in this mix of hydrother- mary production but rather the question crobial symbiont has developed to the mal fluid and bottom seawater may be of the problem of biological activity at an point where all ingestive and digestive quickly consumed biologically as well as upper temperature limit per se. morphological features have been lost. chemically, and both aerobic and anaer- In the early spring of 1984, dense Through an active blood system the ani- obic microorganisms may exist in sub- communities of marine invertebrates mal provides the bacteria in the tropho- surface vent systems. Most aerobic bac- were also discovered at a depth of 3200 some with H2S and free 02. It appears terial isolates obtained from the turbid m at the base of the West Florida Es- that the spontaneous reaction of the two waters emitted by some of the Galapagos carpment, a site without volcanic or geo- dissolved gases is prevented or slowed Rift warm vents were "mesophilic," that thermic activity (45). In this area H2S- by the presence of an HS--binding pro- is, exhibited growth optima at tempera- containing ground water with a salinity tein (48). The isolation of CH4-oxidizing tures of 250 to 35°C (24). "Extremely about one-third higher than that of the bacteria from Calyptogena gill tissue and thermophilic" isolates obtained from the ambient seawater seeps from jointed Riftia trophosome (33) indicates, but cer- various types of shallow and deep hot limestone formations. The types of ani- tainly not conclusively, that chemosyn- vents are all anaerobic with growth mals found here are similar to those thesis by CH4 assimilation (ribulose mo- ranges from 650 to H10°C and growth described from the vent sites of the East nophosphate pathway) may also take optima from 860 to 105°C (40). Most of Pacific Rise, but the individuals as well place. Enzymes associated with both the these isolates belong to the "archaebac- as the total quantities are smaller. The ATP-producing system and the Calvin teria," which are distinguished from the presence of H2S has not been measured, cycle have been found in Riftia and "eubacteria" and from all eukaryotic but it is inferred from the odor of the Calyptogena. Physiological work on pu- 724 SCIENCE, VOL. 229 rified preparations of symbionts from bridge Univ. Press, Cambridge, 1984), vol. 2, Seafloor Spreading Centers, P. A. Rona et al., pp. 123-168. Eds. (NATO Conference Series IV, Plenum, Riftia and the newly described vent mus- 8. K. 0. Stetter and G. Gaag, Nature (London) New York, 1983), vol. 12, pp. 677-709. 305, 309 (1983). 31. J. M. Edmond, personal communication. sel Bathymodiolus thermophilus (49) 9. S. Belkin, C. 0. Wirsen, H. W. Jannasch, Appl. 32. R. Whittenbury and H. Dalton, in The Prokary- showed that their chemoautotrophic ac- Environ. Microbiol. 49, 1057 (1985). otes, M. P. Starr et al., Eds. (Springer, Berlin, 10. J. M. Edmond et al., Earth Planet. Sci. Lett. 46, 1981), vol. 1, pp. 894-902. tivities differ greatly with respect to tem- 1(1979); ibid., p. 19. 33. R. S. Hanson, personal communication. perature and the type of electron donor 11. K. L. Von Damm, thesis, Woods Hole Oceano- 34. G. A. Zavarzin and A. N. Nozhevnikova, Mi- graphic Institution-Massachusetts Institute of crob. Ecol. 3, 305 (1977); Y. Park and G. Hege- used (50). Technology (1983). man, in Microbial Chemoautotrophy, W. R. Probably because of heavy 12. M. J. Mottl, H. D. Holland, R. F. Conf, Geo- Strohl and 0. H. Tuovinen, Eds. (Ohio State chim. Cosmochim. Acta 43, 869 (1979); W. C. Univ. Press, Columbus, 1984), pp. 211-218. of dying vent communities, fossilized Shanks III, J. L. Bischoff, R. J. Rosenbauer, 35. H. G. Schlegel, in Marine Ecology, 0. Kinne, ibid. 45, 1977 (1981). Ed. (Wiley, New York, 1975), vol. 2, pp. 9-60. animal remains in metal-rich deposits of 13. H. Craig, et al., Eos 61, 992 (1980). 36. H. W. Jannasch and D. C. Nelson, in Current ancient sea-floor spreading centers and 14. M. J. Mottl, Geol. Soc. Am. Bull. 94, 161 (1983). Perspectives of , M. J. Klug 15. J. L. Bischoff and W. E. Seyfried, Jr., Am. J. and C. A. Reddy, Eds. (American Society of presently mined ophiolites have only Sci. 278, 838 (1978); R. M. Haymon and M. Microbiology, Washington, D.C., 1984), pp. rarely been found (51). Evidence for Kastner, Earth Planet. Sci. Lett. 53, 363 (1981). 170-176. 16. J. F. Kerridge, R. M. Haymon, M. Kastner, 37. J. A. Baross, M. D. Lilley, L. I. Gordon, Nature microbial activities at similar sites has Earth Planet. Sci. Lett. 66, 91 (1983); M. Arnold (London) 298, 366 (1982). been based on the results of sulfur iso- and S. M. F. Sheppard, ibid. 56, 148 (1981); M. 38. W. J. Jones et al., Arch. Microbiol. 136, 254 M. Styrt et al., ibid. 53, 382 (1981). (1983). tope analyses (52). 17. M. D. Lilly, J. A. Baross, L. I. Gordon, in 39. H. L. Ehrlich, in Microbial Chemoautotrophy, Hydrothermal Processes at Seafloor Spreading W. R. Strohl and 0. H. Tuovinen, Eds. (Ohio The most significant geomicrobiologi- Centers, P. A. Rona et al., Eds. (NATO Confer- State Univ. Press, Columbus, 1984), pp. 47-56; cal point of the deep-sea vent discovery ence Series IV, Plenum, New York, 1983), vol. Ecol. Bull. (Stockholm) 35, 357 (1983). 12, pp. 411-449; M. D. Lilly, M. A. de Angelis, 40. W. Zillig et al., Naturwissenschaften 69, 197 is the dependence of entire L. I. Gordon, Nature (London) 300, 48 (1982); J. (1982); K. 0. Stetter, Nature (London) 300, 258 on geothermal (terrestrial) rather than A. Baross, M. D. Lilly, L. I. Gordon, ibid. 298, (1982); S. Belkin and H. W. Jannasch, Arch. 366 (1982). Microbiol. 141, 181 (1985). solar energy. Were a catastrophic dark- 18. W. E. Seyfried, Jr., and D. R. Janecky, Extend- 41. C. R. Woese, Zentralb. Bakteriol. Parasitenkd. ening of the earth's surface to occur (53), ed Abstracts, Fourth Int. Symp. on Water-Rock Infektionskr. Hyg. I Abt. Orig. C3, 1 (1982). Interaction (International Association of Geo- 42. P. B. Comita and R. B. Gagosian, Science 222, the chance of survival of such ecosys- chemists and Cosmochemists, Misasa, Japan, 1329 (1983). 1983), p. 433; D. R. Janecky and W. E. Seyfried, 43. J. B. Corliss, J. A. Baross, S. E. Hoffman, tems is the highest of any in Jr., ibid., p. 210; Geochim. Cosmochim. Acta, Oceanol. Acta N°SP, 59 (1981). the biosphere. The chemosynthetic exis- in press. 44. P. B. Comita, R. B. Gagosian, P. M. Williams, 19. J. A. Welhan and H. Craig, in Hydrothermal Nature (London) 307, 450 (1984). tence of organisms in the deep sea also Processes at Seafloor Spreading Centers, P. A. 45. C. K. Paull et al., Science 226, 965 (1984). suggests a possible occurrence of similar Rona et al., Eds. (NATO Conference Series IV, 46. K. J. Boss and R. D. Turner, Malacologia 20, Plenum, New York, 1983), vol. 12, pp. 391-409. 161 (1980); M. L. Jones, Proc. Biol. Soc. Wash. life forms in other planetary settings 20. M. J. Mottl and H. D. Holland, Geochim. Cos- 93, 1295 (1980). where water may be present only in the mochim. Acta 42, 1103 (1978). 47. C. M. Cavanaugh et al., Science 213, 340 (1981); 21. J. A. Baross, J. W. Deming, R. R. Becker, in C. M. Cavanaugh, Nature (London) 302, 56 absence of light. It is surprising that, as Current Perspectives of Microbial Ecology, M. (1983); D. C. Nelson, J. B. Waterbury, H. W. J. Klug and C. A. Reddy, Eds. (American Jannasch, FEMS Microbiol. Lett. 24, 267 (1984); far as we know, science fiction writers Society of Microbiology, Washington, D.C., H. Felbeck, J. J. Childress, G. N. Somero, in did not turn their attention to geochemi- 1984), pp. 186-195; J. D. Trent, R. A. Chastain, The Mollusca, P. W. Hochachka, Ed. (Academ- A. A. Yayanos, Nature (London) 307, 737 ic Press, London, 1984), vol. 2, pp. 331-358. cally supported complex forms of life (1984); R. H. White, ibid. 310, 430 (1984). 48. A. G. Arp and J. J. Childress, Science 213, 342 until such forms were actually discov- 22. R. E. McDuff and J. M. Edmond, Earth Planet. (1981); ibid. 219, 295 (1983). Sci. Lett. 57, 117 (1982). 49. V. C. Kenk and B. R. Wilson, Malacologia 26, ered in the deep sea. 23. D. M. Karl, Microbiol. Rev. 44, 739 (1980); 253 (1985). Appl. Environ. Microbiol. 42, 802 (1981); C. D. 50. D. C. Nelson, S. Belkin, H. W. Jannasch, in References and Notes Winn and D. M. Karl, ibid. 47, 835 (1984). pre aration. 24. D. M. Karl et al., Mar. Biol. Lett. 5, 227 (1984). 51. R. M. Haymon, R. A. Koski, C. Sinclair, Sct-- I. D. L. Williams, R. P. von Herzen, J. G. Sclater, 25. E. G. Ruby, C. 0. Wirsen, H. W. Jannasch, ence 223, 1407 (1984). R. N. Anderson, Geophys. J. R. Astron. Soc. Appl. Environ. Microbiol. 42, 317 (1981); E. G. 52. A. J. Boyce, M. L. Coleman, M. J. Russell, 38, 587 (1974); R. F. Weiss, P. Lonsdale, J. E. Ruby and H. W. Jannasch, J. Bacteriol. 149, 161 Nature (London) 306, 545 (1983). Lupton, A. E. Bainbridge, H. Craig, Nature (1982). 53. P. R. Ehrlich et al., Science 222, 1293 (1983). (London) 267, 600 (1977). 26. J. H. Tuttle, C. 0. Wirsen, H. W. Jannasch, 54. H. W. Jannasch and C. D. Taylor, Annu. Rev. 2. J. B. Corliss et al., Science 203, 1073 (1979). Mar. Biol. 73, 293 (1983). Microbiol. 38, 487 (1984). 3. P. F. Lonsdale, Deep-Sea Res. 24, 875 (1977). 27. H. W. Jannasch, in The Microbe 1984, D. P. 55. We thank C. 0. Wirsen, D. C. Nelson, J. B. 4. H. W. Jannasch and C. 0. Wirsen, BioScience Kelly and N. G. Can, Eds. (Cambridge Univ. Waterbury, and S. J. Molyneaux for their col- 29, 592 (1979). Press, Cambridge, 1984), vol. 2, pp. 97-122. laboration in many aspects of this work and J. 5. D. M. Karl, C. 0. Wirsen, H. W. Jannasch, 28. H. W. Jannasch and C. 0. Wirsen, Appl. Envi- M. Peterson for assistance in the preparation of Science 207, 1345 (1980). ron. Microbiol. 41, 528 (1981). the manuscript. Our research is supported by 6. W. Pfeffer, Planzenphysiology (Engelmann, 29. D. C. Nelson, J. B. Waterbury, H. W. Jannasch. National Science Foundation grants OCE82- Leipzig, 1897), vol. 1. Arch. Microbiol. 133, 172 (1982); D. C. Nelson 14896, OCE83-08631 (H.W.J.), and OCE83- 7. R. K. Thauer and J. G. Momris, in The Microbe and H. W. Jannasch, ibid. 136, 262 (1983). 10175 (M.J.M.). Contribution 5764 ofthe Woods 1984, D. P. Kelly and N. G. Carr, Eds. (Cam- 30. H. W. Jannasch, in Hydrothermal Processes at Hole Oceanographic Institution.

23 AUGUST 1985 725